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Mitochondrial Energy-Dissipating Systems (Alternative Oxidase, Uncoupling Proteins, and External NADH Dehydrogenase) Are Involved in Development of Frost-Resistance of Winter Wheat Seedlings

O. I. Grabelnych1*, O. A. Borovik1, E. L. Tauson1, T. P. Pobezhimova1, A. I. Katyshev1, N. S. Pavlovskaya1, N. A. Koroleva1, I. V. Lyubushkina1, V. Yu. Bashmakov2, V. N. Popov2, G. B. Borovskii1, and V. K. Voinikov1

1Siberian Institute of Plant Physiology and Biochemistry, Siberian Division of the Russian Academy of Sciences, ul. Lermontova 132, 664033 Irkutsk, Russia; fax: (3952) 517-054; E-mail: grolga@sifibr.irk.ru

2Voronezh State University, Universitetskaya pl. 1, 394006 Voronezh, Russia; fax: (4732) 208-755; E-mail: popov@vsu.ru

* To whom correspondence should be addressed.

Received August 9, 2013; Revision received December 9, 2013
Gene expression, protein synthesis, and activities of alternative oxidase (AOX), uncoupling proteins (UCP), adenine nucleotide translocator (ANT), and non-coupled NAD(P)H dehydrogenases (NDex, NDPex, and NDin) were studied in shoots of etiolated winter wheat (Triticum aestivum L.) seedlings after exposure to hardening low positive (2°C for 7 days) and freezing (-2°C for 2 days) temperatures. The cold hardening efficiently increased frost-resistance of the seedlings and decreased the generation of reactive oxygen species (ROS) during further cold shock. Functioning of mitochondrial energy-dissipating systems can represent a mechanism responsible for the decrease in ROS under these conditions. These systems are different in their response to the action of the hardening low positive and freezing temperatures. The functioning of the first system causes induction of AOX and UCP synthesis associated with an increase in electron transfer via AOX in the mitochondrial respiratory chain and also with an increase in the sensitivity of mitochondrial non-phosphorylating respiration to linoleic and palmitic acids. The increase in electron transfer via AOX upon exposure of seedlings to hardening freezing temperature is associated with retention of a high activity of NDex. It seems that NDex but not the NDPex and NDin can play an important role in maintaining the functional state of mitochondria in heterotrophic tissues of plants under the influence of freezing temperatures. The involvement of the mitochondrial energy-dissipating systems and their possible physiological role in the adaptation of winter crops to cold and frost are discussed.
KEY WORDS: Triticum aestivum L., cold hardening, reactive oxygen species, gene expression, energy-dissipating systems of mitochondria

DOI: 10.1134/S0006297914060030